IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28590-4.html
   My bibliography  Save this article

ASPP2 maintains the integrity of mechanically stressed pseudostratified epithelia during morphogenesis

Author

Listed:
  • Christophe Royer

    (University of Oxford)

  • Elizabeth Sandham

    (University of Oxford)

  • Elizabeth Slee

    (University of Oxford)

  • Falk Schneider

    (University of Oxford
    University of Southern California)

  • Christoffer B. Lagerholm

    (University of Oxford)

  • Jonathan Godwin

    (University of Oxford
    University of Oxford)

  • Nisha Veits

    (University of Oxford)

  • Holly Hathrell

    (University of Oxford)

  • Felix Zhou

    (University of Oxford)

  • Karolis Leonavicius

    (University of Oxford
    Vilnius University)

  • Jemma Garratt

    (University of Oxford
    University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital)

  • Tanaya Narendra

    (University of Oxford
    University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital)

  • Anna Vincent

    (Oxford Business Park North)

  • Celine Jones

    (University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital)

  • Tim Child

    (University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital
    Oxford Business Park North)

  • Kevin Coward

    (University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital)

  • Chris Graham

    (University of Oxford, Level 3, Women’s Centre, John Radcliffe Hospital)

  • Marco Fritzsche

    (University of Oxford
    Rosalind Franklin Institute)

  • Xin Lu

    (University of Oxford)

  • Shankar Srinivas

    (University of Oxford)

Abstract

During development, pseudostratified epithelia undergo large scale morphogenetic events associated with increased mechanical stress. Using a variety of genetic and imaging approaches, we uncover that in the mouse E6.5 epiblast, where apical tension is highest, ASPP2 safeguards tissue integrity. It achieves this by preventing the most apical daughter cells from delaminating apically following division events. In this context, ASPP2 maintains the integrity and organisation of the filamentous actin cytoskeleton at apical junctions. ASPP2 is also essential during gastrulation in the primitive streak, in somites and in the head fold region, suggesting that it is required across a wide range of pseudostratified epithelia during morphogenetic events that are accompanied by intense tissue remodelling. Finally, our study also suggests that the interaction between ASPP2 and PP1 is essential to the tumour suppressor function of ASPP2, which may be particularly relevant in the context of tissues that are subject to increased mechanical stress.

Suggested Citation

  • Christophe Royer & Elizabeth Sandham & Elizabeth Slee & Falk Schneider & Christoffer B. Lagerholm & Jonathan Godwin & Nisha Veits & Holly Hathrell & Felix Zhou & Karolis Leonavicius & Jemma Garratt & , 2022. "ASPP2 maintains the integrity of mechanically stressed pseudostratified epithelia during morphogenesis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28590-4
    DOI: 10.1038/s41467-022-28590-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28590-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28590-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yu-ichiro Nakajima & Emily J. Meyer & Amanda Kroesen & Sean A. McKinney & Matthew C. Gibson, 2013. "Epithelial junctions maintain tissue architecture by directing planar spindle orientation," Nature, Nature, vol. 500(7462), pages 359-362, August.
    2. Takefumi Kondo & Shigeo Hayashi, 2013. "Mitotic cell rounding accelerates epithelial invagination," Nature, Nature, vol. 494(7435), pages 125-129, February.
    3. M. Teresa Bertran & Stéphane Mouilleron & Yanxiang Zhou & Rakhi Bajaj & Federico Uliana & Ganesan Senthil Kumar & Audrey Drogen & Rebecca Lee & Jennifer J. Banerjee & Simon Hauri & Nicola O’Reilly & M, 2019. "ASPP proteins discriminate between PP1 catalytic subunits through their SH3 domain and the PP1 C-tail," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
    4. Matteo Rauzi & Uros Krzic & Timothy E. Saunders & Matej Krajnc & Primož Ziherl & Lars Hufnagel & Maria Leptin, 2015. "Embryo-scale tissue mechanics during Drosophila gastrulation movements," Nature Communications, Nature, vol. 6(1), pages 1-12, December.
    5. Esteban Hoijman & Davide Rubbini & Julien Colombelli & Berta Alsina, 2015. "Mitotic cell rounding and epithelial thinning regulate lumen growth and shape," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    6. Chuen Yan Leung & Magdalena Zernicka-Goetz, 2013. "Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and -independent mechanisms," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    7. Floris Bosveld & Olga Markova & Boris Guirao & Charlotte Martin & Zhimin Wang & Anaëlle Pierre & Maria Balakireva & Isabelle Gaugue & Anna Ainslie & Nicolas Christophorou & David K. Lubensky & Nicolas, 2016. "Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis," Nature, Nature, vol. 530(7591), pages 495-498, February.
    8. Julie Salomon & Cécile Gaston & Jérémy Magescas & Boris Duvauchelle & Danielle Canioni & Lucie Sengmanivong & Adeline Mayeux & Grégoire Michaux & Florence Campeotto & Julie Lemale & Jérôme Viala & Fra, 2017. "Contractile forces at tricellular contacts modulate epithelial organization and monolayer integrity," Nature Communications, Nature, vol. 8(1), pages 1-18, April.
    9. Floris Bosveld & Olga Markova & Boris Guirao & Charlotte Martin & Zhimin Wang & Anaëlle Pierre & Maria Balakireva & Isabelle Gaugue & Anna Ainslie & Nicolas Christophorou & David K. Lubensky & Nicolas, 2016. "Erratum: Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis," Nature, Nature, vol. 534(7605), pages 138-138, June.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Evangéline Despin-Guitard & Viviane S. Rosa & Steffen Plunder & Navrita Mathiah & Kristof Schoor & Eliana Nehme & Sara Merino-Aceituno & Joaquim Egea & Marta N. Shahbazi & Eric Theveneau & Isabelle Mi, 2024. "Non-apical mitoses contribute to cell delamination during mouse gastrulation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. K. Sri-Ranjan & J. L. Sanchez-Alonso & P. Swiatlowska & S. Rothery & P. Novak & S. Gerlach & D. Koeninger & B. Hoffmann & R. Merkel & M. M. Stevens & S. X. Sun & J. Gorelik & Vania M. M. Braga, 2022. "Intrinsic cell rheology drives junction maturation," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Pénélope Darnat & Angélique Burg & Jérémy Sallé & Jérôme Lacoste & Sophie Louvet-Vallée & Michel Gho & Agnès Audibert, 2022. "Cortical Cyclin A controls spindle orientation during asymmetric cell divisions in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Guilherme Ventura & Aboutaleb Amiri & Raghavan Thiagarajan & Mari Tolonen & Amin Doostmohammadi & Jakub Sedzinski, 2022. "Multiciliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Hannah J. Gustafson & Nikolas Claussen & Stefano Renzis & Sebastian J. Streichan, 2022. "Patterned mechanical feedback establishes a global myosin gradient," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Aurélien Villedieu & Lale Alpar & Isabelle Gaugué & Amina Joudat & François Graner & Floris Bosveld & Yohanns Bellaïche, 2023. "Homeotic compartment curvature and tension control spatiotemporal folding dynamics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Sabrina Meindlhumer & Fridtjof Brauns & Jernej Rudi Finžgar & Jacob Kerssemakers & Cees Dekker & Erwin Frey, 2023. "Directing Min protein patterns with advective bulk flow," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    7. Gautam Srivastava & Meng S. Choy & Nicolas Bolik-Coulon & Rebecca Page & Wolfgang Peti, 2023. "Inhibitor-3 inhibits Protein Phosphatase 1 via a metal binding dynamic protein–protein interaction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Robin M. Skory & Adam A. Moverley & Goli Ardestani & Yanina Alvarez & Ana Domingo-Muelas & Oz Pomp & Blake Hernandez & Piotr Tetlak & Stephanie Bissiere & Claudio D. Stern & Denny Sakkas & Nicolas Pla, 2023. "The nuclear lamina couples mechanical forces to cell fate in the preimplantation embryo via actin organization," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Sarah Lemaire & Mónica Ferreira & Zander Claes & Rita Derua & Madryn Lake & Gerd Hoeven & Fabienne Withof & Xinyu Cao & Elora C. Greiner & Arminja N. Kettenbach & Aleyde Eynde & Mathieu Bollen, 2024. "PPP1R2 stimulates protein phosphatase-1 through stabilisation of dynamic subunit interactions," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Julien Fierling & Alphy John & Barthélémy Delorme & Alexandre Torzynski & Guy B. Blanchard & Claire M. Lye & Anna Popkova & Grégoire Malandain & Bénédicte Sanson & Jocelyn Étienne & Philippe Marmottan, 2022. "Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28590-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.